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Phylogenomic Analyses of More Than 4000 Nuclear Loci Resolve the Origin

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Phylogenomic Analyses of More Than 4000 Nuclear Loci Resolve the Origin Downloaded from http://rsbl.royalsocietypublishing.org/ on September 13, 2017 Evolutionary biology Phylogenomic analyses of more than rsbl.royalsocietypublishing.org 4000 nuclear loci resolve the origin of snakes among lizard families Research Jeffrey W. Streicher1,2 and John J. Wiens1 1Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85721-0088, USA Cite this article: Streicher JW, Wiens JJ. 2017 2Department of Life Sciences, The Natural History Museum, London SW7 5BD, UK Phylogenomic analyses of more than 4000 JWS, 0000-0002-3738-4162; JJW, 0000-0003-4243-1127 nuclear loci resolve the origin of snakes among lizard families. Biol. Lett. 13: Squamate reptiles (lizards and snakes) are the most diverse group of terres- 20170393. trial vertebrates, with more than 10 000 species. Despite considerable effort http://dx.doi.org/10.1098/rsbl.2017.0393 to resolve relationships among major squamates clades, some branches have remained difficult. Among the most vexing has been the placement of snakes among lizard families, with most studies yielding only weak sup- port for the position of snakes. Furthermore, the placement of iguanian Received: 17 June 2017 lizards has remained controversial. Here we used targeted sequence capture Accepted: 18 August 2017 to obtain data from 4178 nuclear loci from ultraconserved elements from 32 squamate taxa (and five outgroups) including representatives of all major squamate groups. Using both concatenated and species-tree methods, we recover strong support for a sister relationship between iguanian and angu- imorph lizards, with snakes strongly supported as the sister group of these Subject Areas: two clades. These analyses strongly resolve the difficult placement of snakes taxonomy and systematics within squamates and show overwhelming support for the contentious pos- ition of iguanians. More generally, we provide a strongly supported Keywords: hypothesis of higher-level relationships in the most species-rich tetrapod clade using coalescent-based species-tree methods and approximately 100 lizards, phylogenomics, snakes, species-tree times more loci than previous estimates. Author for correspondence: Jeffrey W. Streicher 1. Introduction e-mail: [email protected] Squamates, lizards and snakes, are a particularly important group. They include more than 10 000 extant species [1], surpassing birds as the most diverse major tetrapod clade. They are used as study systems in many areas of research, including (among many) the evolution of sex, viviparity, herbivory, body form and toxins [2]. Venomous squamates also pose a serious hazard to humans in some regions [3], whereas their venoms offer many resources for medical research [4]. There has been considerable recent research on higher-level squamate phylogeny, but some branches have remained contentious. Molecular analyses have supported a very different set of relationships relative to those suggested by morphology. Morphological analyses have placed iguanian lizards at the base of the squamate tree [5,6]. By contrast, molecular analyses have placed gekkotans and dibamids at the base, and iguanians in a more recent clade with snakes and anguimorphs [7–11]. Combined analyses of molecular and morphological data have also supported the molecular trees [12,13], and have shown that the support for the morphological tree is problematic. Nevertheless, some authors have continued to question the placement of iguanians by Electronic supplementary material is available molecular data [6,14,15]. online at https://dx.doi.org/10.6084/m9. Further, some key aspects of higher-level squamate phylogeny have remained uncertain, even in molecular analyses. One is the placement of figshare.c.3865459. snakes. Many molecular analyses have placed snakes as the sister to a clade & 2017 The Author(s) Published by the Royal Society. All rights reserved. Downloaded from http://rsbl.royalsocietypublishing.org/ on September 13, 2017 uniting iguanians and anguimorphs, but the support for the analyses used the CIPRES server [24] and branch support was 2 latter clade has been consistently weak [8–11]. Furthermore, assessed with bootstrapping. Species-trees analyses used the pro- rsbl.royalsocietypublishing.org previous studies generally used concatenated analyses, gram ASTRAL 4.10.11 [25,26], with branch support estimated rather than species-tree analyses. Concatenated analyses using local posterior probabilities [27]. may yield weak or even positively misleading results when We generally included only taxa with more than 1000 UCEs. However, we included two more incomplete taxa that were there is extensive conflict among gene trees, whereas potentially important for the tree’s base: the dibamid Anelytropsis species-tree methods can yield well-supported and accurate (90 UCEs; electronic supplementary material, table S1) and the results [16]. Such conflicts among gene trees are well docu- closest squamate outgroup (Sphenodon; 596 UCEs, electronic mented for many major branches of squamate phylogeny supplementary material, table S1). Although Anelytropsis is [9]. Another key area of uncertainty is whether the sister highly incomplete, its inclusion or exclusion had no impact on group to all other squamates is dibamids [7,10,11] or a the estimated topologies (see the electronic supplementary clade consisting of dibamids and gekkotans [9,12,13]. material, figures S1 and S2). Biol. Lett. Here, we analyse higher-level squamate relationships using phylogenomic data and species-tree methods. We obtain nuclear data from 4178 loci, approximately 100 times 13 more than previous analyses of higher-level squamate phylo- 3. Results : 20170393 geny [9,11,13]. We strongly support snakes as the sister group The concatenated and species-tree analyses provided strong of a well-supported clade uniting Iguania þ Anguimorpha. and concordant support for most higher-level squamate Thus, our analyses simultaneously resolve these two persistent relationships (figure 1; electronic supplementary material, controversies in squamate phylogeny. Overall, we provide a figure S3). There was strong support for a clade uniting angu- generally well-supported estimate of higher-level squamate imorphs, iguanians, and snakes (Toxicofera) and strong phylogeny using phylogenomic data and species-tree methods. support for a clade linking anguimorphs and iguanians. Thus, these results strongly resolve the controversial place- ment of snakes and iguanians with species-tree methods and a dataset of unprecedented size. There was strong, 2. Material and methods concordant support for most other relationships across the We sampled 32 squamate species and five outgroup taxa, which tree, such as the clade uniting scincids, xantusiids, gerrho- included representatives of all major amniote clades (i.e. rhyncho- saurids and cordylids (Scincoidea), and the clade uniting cephalians, crocodilians, birds, turtles and mammals). Sampling gymnophthalmids, teiids, lacertids, and amphisbaenians within squamates included all major groups and most families (out- (Lacertoidea). The backbone relationships among these side of snakes, iguanians and amphisbaenians). Details of sampling major clades were also strongly supported. are given in the electronic supplementary material, table S1. There were also a few remaining areas of uncertainty. We used anchored enrichment to sequence ultraconserved Both approaches agreed that dibamids and gekkotans are at elements (UCEs, [17]) and obtained an average of 2738.7 UCEs the base of the squamate tree, but differ as to whether diba- per species. Laboratory methods (following [18,19]) are listed mids are sister to all other squamates (ASTRAL), or whether in the electronic supplementary material, appendix S1. Data for dibamids and gekkotans are sister taxa (concatenated). The most outgroups (all but Sphenodon) and nine ingroup taxa were from previous studies (electronic supplementary material, conflicting relationships were moderately supported by table S1). We obtained new UCE data for 24 taxa. In theory, each approach. There were also conflicts (and weak support we could have included additional published data for iguanian from ASTRAL) among some gekkotan families. Finally, lizards [18] and snakes [19]. However to make the analyses there were conflicting results and weak support regarding more computationally tractable, we included only three species monophyly of amphisbaenians relative to lacertids. from each clade, representing major lineages (i.e. scolecophidian, pythonid, and colubroid snakes; pleurodont and acrodont iguanians). We included the most complete taxon available within each major lineage. 4. Discussion We cleaned, assembled, identified and aligned UCE data In this study, we assembled a large phylogenomic dataset to using the software packages velvet 1.2.10 [20] and PHYLUCE address higher-level squamate phylogeny, using species-tree 2.0.0 [17,21]. We included UCEs with up to 50% missing taxa, which appears to give optimal results [18]. The final dataset methods and sampling approximately 100 times more loci had 4178 UCEs (1 530 015 total aligned base pairs), with 52.4% than previous studies. Our results strongly resolve the phylo- missing data overall (including gaps). The average number of genetic placement of snakes among lizard families, as the variable sites per UCE was 108.3 (range 17–455) and mean sister group to anguimorphs and iguanians. Concomitantly, UCE length was 380.0 base pairs (range 108–878). Raw FASTQ they provide overwhelming evidence to conclusively
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